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A Genetic Framework for Regulation and Seasonal Adaptation of Shoot Architecture in Hybrid Aspen

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A Genetic Framework for Regulation and Seasonal Adaptation of Shoot Architecture in Hybrid Aspen A genetic framework for regulation and seasonal adaptation of shoot architecture in hybrid aspen Jay P. Mauryaa,b, Pal C. Miskolczia, Sanatkumar Mishraa, Rajesh Kumar Singha, and Rishikesh P. Bhaleraoa,1 aUmeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, SE-901 87 Umeå, Sweden; and bDepartment of Botany, Institute of Science, Banaras Hindu University, Varanasi 221005, Uttar Pradesh, India Edited by Ronald R. Sederoff, North Carolina State University, Raleigh, NC, and approved April 14, 2020 (received for review March 14, 2020) Shoot architecture is critical for optimizing plant adaptation and time–related transcription factor RAV1 has been validated in productivity. In contrast with annuals, branching in perennials branching in trees (17–19). However, information on branching native to temperate and boreal regions must be coordinated with control in perennials is fragmented, and there is a significant gap seasonal growth cycles. How branching is coordinated with in our knowledge of how branching is controlled and integrated seasonal growth is poorly understood. We identified key compo- with seasonal growth cycles in perennial trees (20). Therefore, nents of the genetic network that controls branching and its using functional genetic approaches, we elucidated the genetic regulation by seasonal cues in the model tree hybrid aspen. network that mediates control of branching and its regulation by Our results demonstrate that branching and its control by sea- seasonal cues in the model tree hybrid aspen. These studies re- sonal cues is mediated by mutually antagonistic action of aspen veal the key role played by the mutually antagonistic action of orthologs of the flowering regulators TERMINAL FLOWER 1 LAP1 and TFL1 in mediating control of branching and its re- (TFL1)andAPETALA1 (LIKE APETALA 1/LAP1). LAP1 promotes sponses to hormonal and seasonal cues. Our results show that branching through local action in axillary buds. LAP1 acts in a components involved in photoperiodic control of seasonal cytokinin-dependent manner, stimulating expression of the cell- growth have been recruited along with tree orthologs of pre- AIL1 BRANCHED1 cycle regulator and suppressing expression to viously described branching regulators to control of branching promote branching. Short photoperiod and low temperature, the and its adaptation to seasonal changes. major seasonal cues heralding winter, suppress branching by si- multaneous activation of TFL1 and repression of the LAP1 path- Results DEVELOPMENTAL BIOLOGY way. Our results thus reveal the genetic network mediating Bud Dormancy- and Activation-Related Genes Are Differentially control of branching and its regulation by environmental cues fa- Expressed during Axillary Bud Outgrowth. To identify how shoot cilitating integration of branching with seasonal growth control in branching is regulated in trees, we monitored the temporal ex- perennial trees. pression of genes in axillary buds of hybrid aspen (P. tremula × tremuloides) clone T89 before and after decapitation of shoot shoot architecture | branching | seasonal growth | perennial trees | apex (21) (SI Appendix, Fig. S1). We selected genes previously hybrid aspen implicated in bud dormancy and bud break (both apical and axillary buds). The first visible signals of activity in the buds were hoot architecture has a central role in adaptation and opti- detected 24 to 48 h after decapitation, as buds appeared to grow Smizing plant productivity. Hence the outgrowth of axillary and separate from the stem. Transcript levels of genes previously buds is tightly regulated in response to endogenous signals and implicated in bud outgrowth, such as BRANCHED1/TEOSINTE exogenous environmental cues. Branching has been extensively Arabidopsis studied in the model plants and pea. These studies Significance have shown tight regulation of axillary bud outgrowth, revealed the key genetic components controlling branching, and identified Control of branching is critical for optimizing growth and ad- roles played by hormonal and nutrient signals (1–3). The plant aptation in plants. In contrast with annuals, in perennial plants hormones strigolactone and indole-acetic acid (IAA/auxin) sup- growing in temperate and boreal regions, branching must be press branching, whereas cytokinin and nutrients such as nitrogen controlled temporally to adapt to seasonal changes. The mo- and sucrose promote it (4–13). Hormonal and nutrient signaling lecular pathways regulating branching and its adaptation to pathways converge on transcription factor BRANCHED1 (BRC1) seasonal changes are not well understood in perennial plants. (2, 14), which integrates the various inputs and mediates control of ’ We identified the genetic network underlying the control of branching by regulating axillary buds potential to grow. branching and elucidated its role in branching by seasonal In contrast with annuals, perennials, particularly of boreal and cues in model tree hybrid aspen. Our results reveal compo- temperate regions, face extreme annual variation in temperature nents mediating photoperiodic control of growth in trees, and day length. Essential adaptations of perennials to these and conserved branching regulators have been integrated seasonal changes include synchronized cycles of growth and into a genetic network to control branching and facilitate its dormancy. Prior to winter, shoot growth is arrested and shoot adaptation to seasonal changes experienced by long-lived apical meristems and arrested leaf primordia are enclosed within perennial plants. an apical bud, and precocious activation of shoot growth is prevented by the establishment of dormancy (15, 16). Like shoot Author contributions: J.P.M. and R.P.B. designed research; J.P.M., P.C.M., S.M., and R.K.S. growth, branching needs to be tightly controlled to adapt to performed research; R.P.B. contributed new reagents/analytic tools; J.P.M. and R.P.B. seasonal changes. Inadvertent activation of axillary bud out- analyzed data; and J.P.M. and R.P.B. wrote the paper. growth, late in the season, would cause fatal damage in newly The authors declare no competing interest. formed shoots from early winter frost. This article is a PNAS Direct Submission. Whereas branching is well studied in annual models like Published under the PNAS license. Arabidopsis and pea, much less is known about control of 1To whom correspondence may be addressed. Email: [email protected]. branching in perennial trees. Changes in gene expression in ax- This article contains supporting information online at https://www.pnas.org/lookup/suppl/ illary buds have been described, and the role of a few compo- doi:10.1073/pnas.2004705117/-/DCSupplemental. nents including strigolactones, BRC1 orthologs, and flowering- www.pnas.org/cgi/doi/10.1073/pnas.2004705117 PNAS Latest Articles | 1of8 Downloaded by guest on September 26, 2021 BRANCHED1, CYCLOIDEA, PCF 18 (BRC1/TCP18, a homolog the branching phenotype (SI Appendix, Fig. S5). In contrast with of Arabidopsis BRANCHED 1)(22,23),andTERMINAL FLOWER FT overexpression, LAP1 overexpression led to a significant in- 1/CENTRORADIALIS 1 (TFL1/CEN1) (24) were down-regulated. crease in branching with outgrowth from nearly all of the axillary In contrast, transcript levels of AINTEGUMENTA-LIKE 1 (AIL1), buds (Fig. 2 A and B). a known cell proliferation regulator (25–27), and Arabidopsis The up-regulation of LAP1 expression in TFL1-RNAi axillary thaliana HISTIDINE PHOSPHOTRANSMITTER 4 (AHP4, puta- buds and the LAP1oe phenotype suggested that TFL1 sup- tively involved in cytokinin signaling) (28) were up-regulated 8 to presses axillary bud outgrowth by suppressing LAP1 expression. 24 h after shoot apex decapitation before any visible change in To test this hypothesis, we generated TFL1-RNAi aspen plants SI Appendix A–D axillary buds ( ,Fig.S2 ). Thus, genes implicated in with LAP1 activity knocked out by clustered regularly inter- bud dormancy and outgrowth display dynamic changes in expres- spaced short palindromic repeats (CRISPR)-Cas9 (Fig. 2C and sion preceding and during axillary bud outgrowth. SI Appendix, Fig. S6). The resulting TFL1-RNAi/LAP1ko plants TFL1/CEN1 resembled WT producing extremely few branches, in contrast Is a Branching Repressor. The correlation between down- LAP1 regulation of TFL1 expression preceding axillary bud outgrowth with TFL1-RNAi plants. Thus, loss of function of could and its proposed role as a negative regulator of apical bud break suppress increased branching resulting from down-regulation of TFL1 LAP1 (SI Appendix, Fig. S2B) (24) prompted us to investigate its role in . The enhanced expression of in TFL1-RNAi and axillary bud outgrowth. RNA interference (RNAi)-mediated suppression of branching in TFL1-RNAi by loss of function of down-regulation of TFL1 (SI Appendix, Fig. S3) resulted in more LAP1 indicate that LAP1 is a downstream target in TFL1- branching than in wild-type (WT) plants (Fig. 1A). Moreover, mediated control of branching. upon decapitation, TFL-down-regulated (TFL1-RNAi) and -overexpressing (TFL1oe) lines had significantly higher and LAP1 Acts Locally in Promoting Branching by Modulating Key lower frequencies of axillary bud outgrowth, respectively, than Branching-Related Genes. Following identification of the role of WT plants (SI Appendix, Fig. S4 A and B). These results suggest LAP1 in branching, we investigated if LAP1 acts locally or sys- that TFL1 acts to repress branching in hybrid aspen. temically
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